Avances en Investigación Agropecuaria ISSN: 0188-7890 [email protected] Universidad de Colima México

Current knowledge of the cichlid fishes of the Amacuzac River, Mexico

Franco Archundia, Marco Polo; Arce Uribe, Elsah; Luna-Figueroa, Jorge Current knowledge of the cichlid fishes of the Amacuzac River, Mexico Avances en Investigación Agropecuaria, vol. 22, no. 2, 2018 Universidad de Colima, México Available in: https://www.redalyc.org/articulo.oa?id=83757609006 AVANCES EN INVESTIGACIÓN AGROPECUARIA, volumen 22, suplemento 1, octubre 2018 es una Publicación cuatrimestral editada por la Universidad de Colima, Av. Universidad # 333, Col. Las Víboras, Colima, Colima, México. CP 28045. Teléfono: (312) 3161000. Ext. 40011, www.ucol.mx/revaia, [email protected], [email protected]. Director responsable José Manuel Palma García. Reserva de Derechos al Uso Exclusivo No. 04-2016-112411015200-203, ISSN digital "en trámite", ambos otorgados por el Instituto Nacional del Derecho de Autor. Responsable de la última actualización, MC. Rosa Alejandra del Viento Camacho e Ing. Manuel Gutiérrez Gómez, Av. Universidad # 333, Col. Las Víboras, Colima, Colima, México. CP 28045, fecha de última modificación 10 de octubre de 2018.

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Artículo de revisión Current knowledge of the cichlid fishes of the Amacuzac River, Mexico Conocimiento actual de los peces cíclidos del río Amacuzac, México

Marco Polo Franco Archundia Redalyc: https://www.redalyc.org/articulo.oa? Centro de Investigaciones Biológicas. Universidad id=83757609006 Autónoma del Estado de Morelos, México

Elsah Arce Uribe Centro de Investigaciones Biológicas. Universidad Autónoma del Estado de Morelos, México [email protected]

Jorge Luna-Figueroa Centro de Investigaciones Biológicas. Universidad Autónoma del Estado de Morelos, México Received: 22 June 2018 Accepted: 07 November 2018

Resumen:

La introducción de especies ajenas a un ambiente puede generar cambios en el ecosistema y en la dinámica de los organismos que lo habitan. En el río Amacuzac, México, actualmente se encuentran establecidas cinco especies de cíclidos, de las cuales, cuatro son no nativas: la tilapia de Mozambique (Oreochromis mossambicus), el pez convicto (Amatitlania nigrofasciata), el pez falso boca de fuego (orichthys maculipinnis) y el terror verde (Andinoacara rivulatus). La mojarra criolla (Cichlasoma istlanum) es un cíclido nativo de la cuenca del Balsas a la cual pertenece la subcuenca del río Amacuzac y es utilizada como un recurso pesquero. En este trabajo se realizó una revisión sobre el estado de conocimiento de estas cinco especies de cíclidos habitantes del río Amacuzac. Las especies no nativas son los peces más estudiados mientras que la especie nativa ocupa el penúltimo lugar en el número de investigaciones realizadas. El mayor número de estudios de especies no nativas exige una mayor investigación de la especie nativa que permita la conservación y el manejo de este recurso. Palabras clave: Cíclidos, revisión, peces exóticos, peces nativos, cuenca del Balsas. Abstract:

Introduction of non-native species into an environment can produce changes in the ecosystem and in the dynamic of the organisms that inhabit it. In the Amacuzac River, Mexico, there are currently established, five cichlids species, four of them are non- native: Mozambique tilapia (Oreochromis mossambicus), convict fish (Amatitlania nigrofasciata), spotcheek cichlid (orichthys maculipinnis), and the green terror (Andinoacara rivulatus). e Mexican mojarra (Cichlasoma istlanum) is a native cichlid from the Balsas River basin that belongs to the subbasin of the Amacuzac River, and is used as a fishing resource. In this work, a review of the knowledge about this five cichlid species of the Amacuzac River was done. e non-native species are the most studied fish and the native species has the penultimate place in the number of research. e biggest number of studies about non-native species demands a bigger research about the native species that allows the conservation and management of this resource. Keywords: Cichlids, review, non-native fish, native fish, Balsas’s basin.

Introduction

Introducing new species into the environment brings changes to the ecosystem and to the dynamic of the organisms that live there (Villanueva and Roig, 1995; Traveset and Santamaria, 2004; Leprieur et al., 2006). Survival, behavior, physiology and morphology of native species can be modified if a non-native species is introduced (Lassuy, 1995; Simon and Townsed, 2003; Raymond et al., 2015). Some research have even point out the reduction of the population or even the extinction of native species when non-native species arrive

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(Mooney and Cleland, 2001; Mendoza-Alfaro et al., 2011). For example, in fish, tilapias have been reported as invaders in places where they have been introduced (Canonico et al., 2005). Nilotic tilapia, Oreochromis niloticus (Linnaeus, 1758), displaced the red moon fish, Lepomis miniatus (Jordan, 1877), from the Mexican Gulf estuaries, which was their original habitat (Martin et al., 2010). In the same way, the Mozambique tilapia, Oreochroms mossambicus (Peters, 1852), has been reported asan invader in freshwater, marine and estuarine water (Canonico et al., 2005). Mozambique tilapia was introduced in to the Amacuzac River in Morelos, Mexico. is river is one of the 12 sub-basins that include the hydrological region of the Balsas basin in central Mexico (Toledo and Bozada, 2002). Amacuzac River’s path is 240 km long, and until 2016 there were seven native species of fish and 12 non-native ones (Rosales, 2016). e presence of non-native fish demands a larger research in the na-tive species populations and communities that can help the conservation of native resources from the basin (Schofield and Lous, 2015). In the Cichlid family, Mexican mojarra, Cichlasoma istlanum (Jordan and Snyder, 1899) is the only native cichlid in the Amacuzac River (Danko, 1991) and nowadays coexists with four non-native members from the same family (Mejía-Mojica et al., 2012). In many communities, artisanal fishery of this cichlid has decreased drastically, finding increasingly smaller catches and with smaller organisms (Luna-Figueroa, 2007). Mexican mojarra is part of the daily diet of the communities near this river and they depend on capturing them from their natural environment. Despite several attempts for reintroducing this fish into their natural environment, there is no management and/or reintroduction strategy to the natural environment for this native resource. e most abundant non-native cichlid in the Amacuzac River is the convict fish, Amatitlania nigrofasciata (Günther, 1867), with an abundance of 52.42 % followed by the Mozambique tilapia with 16.25 %, spotcheek cichlid, orichthys maculipinnis (Meek, 1904) with 12.45 % and the green terror, Andinoacara rivulatus (Günther, 1860) with 9.90 %, meanwhile the Mexican mojarra represents just 8.9 7 % of the cichlids (Rosales, 2016). In Mexico the convict fish, the spotcheek cichlid, and the green terror are used as ornamental fish, and the Mozambique tilapia is used for meat production (Mejía-Mojica et al., 2012). Mexican mojarra is used as food resource and its maintenance and reproduction in captivity has been investigated (Luna- Figueroa and Figueroa, 2000). In this paper we revised the knowledge that exists about cichlids from the Amacuzac River. e bibliographic search was done in Google Scholar, using the species key words and their common name. Researches were classified in categories depending on their topic, but almost all the research is focused on the way the tilapia is managed, and the convict fish behaviour (table 1).

TABLE 1 Researches conducted in the cichlids of the Amacuzac River (1954-2017).

A) Total researches, B) water quality, C) behavior and chemical signs, D) feeding and growth, E) genetic and reproduction, F) descriptive and population, G) health.

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Anthropogenic importance

e most studied cichlid is the Mozambique tilapia with 1,018 researches because of the importance this fish has as an organism for human consumption. e category with more studies of this fish was health, with 35.85% due to the relevance of their potential zoonosis (Barson et al., 2008), parasites (Madanire-Moyo et al., 2011), and the possible presence of heavy metals in their meat (Liao et al., 2003). Categories such as management and water quality (17.58 %), feeding and growth (17.39 %) were also a high percentage of the researches of this organism with commercial importance (table 1). e convict fish was the second cichlid with more studies, with more than 90 researches (table 1). e use of this fish as an ornamental animal has taken it to be introduce in several countries (Piazzini et al., 2010) and it’s a potential invader organism (Ishikawa and Tachihara, 2010) that has been used to explain the possible processes of non-native fish invasion (Chapple et al., 2012). e fewest studied fish in the anthropogenic importance area is the green terror, with 19 researches and the spotcheek cichlid with one; both of them are used as ornamental species. e Mexican mojarra was the penultimate less studied cichlid, with eight re searches (table 1); this fish is used as a fishing resource for human consumption (Luna-Figueroa et al., 2003), and could be used for culture and reproduction, like the Mozambique tilapia. e management of the Mexican mojarra in captivity could be a mechanism that allows recovering the population on their natural environment and increases the researches of the commercial importance. Today there is no strategy of management for this fish or to reintroduce it to their natural environment.

Behavior and chemical signs

Behavior changes have been identified as an important factor to explain invasion processes (Holway and Suarez, 1999; Chapple et al., 2012; Capelle et al., 2015). Cichlid family presents parental care, territoriality, complex courtship and a remarked social organization, that’s why they have been used as behavior models and to measure the chemical signaling between them (Barlow, 1974; Pollen et al., 2007; Keller-Costa et al., 2015). From the cichlids living in the Amacuzac River, the convict fish could be the fish that has the highest levels of aggression (Ratnasabapathi et al., 1992). is fish was the second cichlid with more studies (90 researches); 67.77 % focused on their behavior and chemical signs (table 1). It’s used as a biological model to study aggressive behavior (Chee et al., 2013) and sexual selection in monogamous species (Noonan, 1983). e Mexican mojarra coexist with four cichlid species in the Balsas basin, and even though they have been observed fighting for shelters (personal observations), nowadays their competitive interactions are unknown. On the other hand, the reproductive behavior of the convict fish has been studied (Wisenden, 1995), finding that feeding affects in reproduction and in parental care (Town-shend and Wootton, 1984). Additionally, the sexual selection of convict fish females has been evaluated focusing in the male’s size and competitive ability (Gagliardi-Seeley et al., 2009). Other studies have reported that Mozambique tilapia male produce sounds during courtship and reproduction (Amorim et al., 2003) and that the jaw structure and the fins (dorsal and anal) of this fish are the most important features for having success in reproduction (Oliveira and Almada, 1995). As for the others cichlids, the green terror and the spotcheek cichlid, their reproductive behavior have not been studied. e Mexican mojarra has been reproducing in laboratory and the frequency of spawning in captivity has been described (Luna-Figueroa and Figueroa, 2000). However their behavior mechanisms related with reproduction are still unknown. As for the studies on social hierarchy, they have found that dominant convict fish grew faster than the subordinates (Lee et al., 2011) and they present a reversion in dominance associated to the formation of reproductive couples (Gagliardi-Seeley, 2012). It has been proven that those changes in the acoustics of

PDF generated from XML JATS4R by Redalyc Project academic non-profit, developed under the open access initiative 57 Avances en Investigación Agropecuaria, 2018, vol. 22, no. 2, May-August, ISSN: 0188-7890 the environment affect the foraging and how they use shelter (McLaughlin and Kunc, 2015), and that the presence of a predator increases parental care (Zworykin, 2011). On the other hand, the chemical compounds segregated by the dominant male of the Mozambique tilapia, determines the hierarchical decisions in these animals (Barata et al., 2007), and as the convict fish, this cichlids present reversion in dominancy (Oliveira and Almada, 1996). As for the green terror, the Mexican mojarra and the spotcheek cichlid, their hierarchical behavior hasn’t been studied. e Mexican mojarra represents a great field for behavior researches, and this could give knowledge to captivity management in a more efficient way, for example, in position in hierarchy maintenance, intraspecific competition, and sexual selection.

Growth, water quality, and health

Fish growing is one of the most studied aspects because it is a good indicator of the orga-nisms health that is determined by the amount and quality of the food and for the physic and chemical characteristics of the water (Cerdá, 2016; Gabriel et al., 2017). Feeding and growth in the different stages of the Mozambique tilapia represent an intensive research all over the years (Rana, 1985; Olvera-Novoa et al., 1990; El-Dahhar and Lovell, 1995; Olvera-Novoa et al., 1998; Keshavanath et al., 2004; Gabriel et al., 2017). Growth and morphological changes patterns of the green terror have been studied (Moshayedi et al., 2017). Probiotics that stimulate growing have been used in the convict fish (Mohammadi et al., 2015; Ramezani and Moghaddasi, 2017). e spotcheek cichlid doesn’t have feeding and growing researches, and the Mexican mojarra, has three (Luna-Figueroa and Benítez, 1999; Luna-Figueroa and Figueroa, 2003; Luna-Figueroa, 2007). Mozambique tilapia is the cichlid with more researches in health, water quality, feeding and growing categories. ere are studies on metals found in their meat, such as Cadmium, Copper, Mercury, Arsenic, and Silver (Pelgrom et al., 1995; Tsai et al., 1995; Liao et al., 2003; Govindasamy and Rahuman, 2012), and also different parasites and diseases (Kaneko et al., 1988; Madanire-Moyo et al., 2011; Firmat et al., 2016). e convict fish and the green terror have researches about parasites found in different parts of their body, for example gills, intestine, and liver (Salgado-Maldonado, 2008; Luque et al., 2016). e Mexican mojarra has been found parasitized in the base of the pectoral fins by the parasite Philometra poblana (Caspeta- Mandujano et al., 2009), and there are not researches focused on the detection or treatment of diseases or metal presence in this animals. e spotcheek cichlid does not even have health studies. From the Mozambique tilapia we know characteristics related with the water quality needed for their culture, such as salinity, temperature, sedimentation, and dissolved solids (Villegas, 1990; Fiess et al., 2007; Arain et al., 2008; Zikos et al., 2014). From the convict fish we just know factors like metabolic rate and oxygen consumption (Fidhiany and Wincler, 1998), the stress of the green terror has been studied in situations of oxygen absence (Neissi et al., 2015). From the Mexican mojarra basic requirements for it culture are known, like physical and chemical water parameters, and there is just one study about thermal preference (Luna-Figueroa et al., 2003). e spotcheek cichlid doesn’t have any research about water quality.

Management and biological researches

Fish used as ornamental organisms and for meat production, represent research fields with relevant economical interest (Melamed et al., 2002). Management in captivity of these organisms is one of the most studied factors (Tanaka et al., 2003). e characteristics that delimitate a good fish management could represent the success or failure of it. In this work, the total researches were divided in management and

PDF generated from XML JATS4R by Redalyc Project academic non-profit, developed under the open access initiative 58 Marco Polo Franco Archundia, et al. Current knowledge of the cichlid fishes of the Amacuzac River,... biological researches. It was considered as management research, the papers that were oriented to culture, and fish maintenance. Biological researches were based on papers on the species’ biology (figure 1). Mozambique tilapia presented 763 management and 255 biological researches. e convict fish had 18 management researches and 72 biological. e green terror had ten management and nine biological researches. Mexican mojarra actually presents five management and three biological researches, and the spotcheek cichlid only had a biological study (figure 1).

FIGURE 1 Biological and management researches of cichlid fish of the Amacuzac River. SC: Spotcheek cichlid, MM: Mexican mojarra, GT: Green terror, CF: Convict fish, and MT: Mozambique tilapia. e size diameter of the circles indicates the total of researches of each species (1954-2017).

Conclusions

ree of the non-native fish species (Mozambique tilapia, convict fish, and green terror) showed more researches than the native species (Mexican mojarra) and just one non-native species (spotcheek cichlid) showed less. ese researches are focused in the importance that this species have to men, either by being organisms used for food, as ornaments or by potential invaders. e researches presented in this paper could show how the native species develops in their natural state, however, it is essential to do more studies about the Mexican mojarra in order to propose a management strategy for the species. e biggest number of researches about non-native species in the Amacuzac River, demands a bigger research of the native species that allows the conservation of it. e wildlife conservation organizations need biological and ecological information in order to make decisions about native and non native species.

Acknowledgements

We thank José Figueroa, Judith García, and Humberto Mejía for helpful comments. We particularly thank the CONACYT Program for providing a full scholarship to Marco Polo Archundia. anks to Lovie Sabugo for editing this english-language text.

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Appendix

Título: Cíclidos de modelos Autora: Marisol Herrera Sosa Técnica: Acuarela Dimensiones: 14.5 x 19.5 cm

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